Different controls on the Hg spikes linked the two pulses of the Late Ordovician mass extinction in South China

The Late Ordovician mass extinction (LOME, ca. 445 Ma; Hirnantian stage) is the second most severe biological crisis of the entire Phanerozoic. The LOME has been subdivided into two pulses (intervals), at the beginning and the ending of the Hirnantian glaciation, the LOMEI-1 and LOMEI-2, respectively. Although most studies suggest a rapid cooling and/or oceanic euxinia as major causes for this mass extinction, the driver of these environmental changes is still debated. As other Phanerozoic’s mass extinctions, extensive volcanism may have been the potential trigger of the Hirnantian glaciation. Indirect evidence of intense volcanism comes from Hg geochemistry: peaks of Hg concentrations have been found before and during the LOME, and have all been attributed to global volcanism in origin. Here, we present high-resolution mercury (Hg) profiles in three study sections, from a shelf to slope transect, on the Yangtze Shelf Sea (South China) to address the origin of Hg anomalies across the Ordovician–Silurian (O–S) boundary. The results show Hg anomaly enrichments in the middle Katian, late Katian, the LOMEI-1 at the beginning of the Hirnantian glaciation, the LOMEI-2 in the late Hirnantian glaciation, and late Rhuddanian. The Hg anomaly enrichments during the middle–late Katian and late Rhuddanian would probably reflect a volcanic origin. We find two different controls on the recorded Hg anomalies during the extinction time: i.e., primarily volcanism for the Hg anomaly at the LOMEI-1 and euxinia for the Hg anomaly at the LOMEI-2. Expansion of euxinia at the LOMEI-1 would have been probably enhanced by volcanic fertilization via weathering of volcanic deposits during the Middle and late Katian, and combined with euxinia at the LOMEI-2 to finally be responsible for the two pulses of the LOME.

Sedimentary Hg has been increasingly used as a tracer for volcanic activity during mass extinction events (e.g., ref. 25 ). Volcanism is the primary sources of atmosphere Hg before the Anthropocene 26 and, given its short residence time in the atmosphere, gaseous volcanic Hg is easily transported and deposited in different depositional environments globally 25,27 . Therefore, sedimentary Hg can be used as a proxy for volcanism 25,[28][29][30][31] . However, increases of Hg deposition in different depositional setting can be also linked to other (local) factors, such as increase of riverine Hg transport to marine settings 32 , massive oxidation of terrestrial organic matter 16,31 , and development of euxinic conditions 33 . Hence, a peak of Hg concentration in the sedimentary record does not unequivocally indicate massive coeval volcanic activity.
In this study, we present new Hg concentration data across the Ordovician-Silurian boundary from three sections at Shuanghe, Qiliao and Tianba on the Yangtze Shelf Sea in South China 4,14 . Combined with previous data on redox conditions and climate changes from the same outcropped sections 4 , these Hg data are used to explore Hg deposition during the LOME in the study area, shedding new light on the origin of the Hg peaks coeval to the biological and environmental changes.

Geological setting
During the Ordovician-Silurian transition, the Yangtze Platform (South China Block) was located near the equator 34 (Fig. 1). After the middle Katian, it gradually evolved into a siliciclastic-dominated shelf basin, called the Yangtze Shelf Sea 4,35 . The shale strata, which include the Late Ordovician Wufeng Formation and early Silurian Lungmachi Formation, or Wufeng-Lungmachi Shale, deposited on the shelf with deepening northwards to the Panthalassic Ocean 4,36,37 . The bottom black shale interval of Wufeng-Lungmachi Shale in South China corresponds to typical, organic-rich shales (hot shale, i.e., more radioactive shale) 7,38 . Owing to the glaciation, a rapid sea level drop occurred during the Hirnantian. Paleo-water-depth in the Yangtze Shelf Sea during this glaciation was likely about 40-100 meters 37 . The Kuanyinchiao Bed at the top of the Wufeng Formation was formed during this glaciation time (Fig. 2), and contains characteristic cold water Hirnantian fauna. The marine carbonate Kuanyinchiao Bed is widely distributed, and has a conformity contact with the underlying Wufeng Formation in the study area. High-resolution graptolite zones have been previously identified in South China 39 , providing a solid biostratigraphic framework and allowing correlation with other Ordovician-Silurian boundary sections around the world 7 .
From the Late Ordovician to early Silurian, volcanic ash layers deposited are extensively reported, especially in North America 40 and South China [41][42][43] . In North America, over 100 volcanic ash layers dominantly occurred in pre-late Katian stage 40 . There were two pulses of volcanic ash layers deposited in South China in the Late Ordovician and early Silurian 42 . The first pulse occurred in late Katian stage 41,42,44 and the second pulse erupted around the boundary between the Rhuddanian stage and the Aeronian stage (ca. 440.8 Ma) 42,45 .

Materials and methods
Fresh rock samples were collected from three sections (Shuanghe, Qiliao and Tianba sections) that were deposited from proximal to distal areas on the Yangtze Shelf Sea, South China (Fig. 1). For each section, high-resolution graptolite zones have been previously defined 4 . Previous studies have reported, from the same rock samples, TOC contents, C-isotopes, Fe-speciation, major elements and trace elements concentrations 4,12,46 . In this study, we measured Hg concentration and TS content of all samples, and the TOC content of 6 new samples.
Hg concentration was measured using a Lumex RA-915 M mercury analyzer with pyrolyzer PYRO-915 + at State Key Laboratory of Biogeology and Envionmental Geology, China University of Geosciences. An aliquot of ~ 50 mg of powdered sample was weighed in a glass boat and was heated in the pyrolyzer at 700 °C. Volatilized     www.nature.com/scientificreports/ Hg concentration was quantified via atomic absorption spectrometry. A soil standard (GSD-17a; Hg = 120 ± 10) was used to calibrate the instrument. Repeated measurements of the standard at the start of each run and throughout the analysis sequence indicate reproducibility was generally better than 10% for Hg concentrations. For the measurement of TOC content, sample powders (2 g) were decarbonated with HCl (10% vol/vol) prior to TOC analyses on a LECO CS-230 analyzer. TS was measured directly by bulk sample. Analytical precision was generally better than 5% and 8% for TOC, and TS contents, respectively. Hg concentrations have been normalized for TOC and TS contents 25,33 .

Discussion
Hg host and digenesis. Hg concentrations in sediments are controlled mainly by local depositional environment, primary volcanic loading, and post depositional diagenesis 47 . In general, Hg is mainly associated with organic matter under "normal" conditions and with sulfide only under strong euxinic conditions 28,47,48 . Hg/TOC or Hg/TS ratios are then used to assess the excess input of Hg besides of the sources from Hg-TOC complexes or HgS 33,48,49 .
Cross-plots between TOC and Hg (Fig. 3) show that Hg concentrations have no correlation with TOC contents under euxinic environments but have positive correlation (R 2 is 0.5 to 0.73, Qiaoliao and Tianba sections) or weak correlation (R 2 = 0.18, Shuanghe section) with TOC contents under non-euxinic environments. It suggests that organic matter is an important host of Hg in these marine sedimentary rocks owing to the association between Hg and organic matter and the reactive Hg organic complexes 50 . Cross-plots between TS and Hg (Fig. 3) show strong correlation (R 2 = 0.81, Qiaoliao section) to no correlation (R 2 is less than 0.31, Shuanghe and Tianba sections) under euxinic environments, but show no correlation under non-euxinic environments. This suggests that sulfide is not a host of Hg under non-euxinic conditions but may be a host of Hg during euxinic intervals 48 .
Normalization of Hg concentrations to TOC and TS can reflect Hg anomalies. Hg/TOC ratios could be inflated because of diagenetic degradation of organic matter, which lowers TOC content 22 , or due to analytical uncertainty for TOC < 0.2% 51 . Therefore, high Hg/TOC ratios in the upper Linxiang Formation of the middle Katian at Shuanghe and Tianba (Table 1) do not indicate true positive Hg anomalies, but are linked to very low TOC values (< 0.1%), and are not plotted in Fig. 2. However, the high Hg/TOC ratios in the lowermost Wufeng Formation are associated with TOC contents higher than 0.2%, suggesting true Hg positive anomalies in the middle Katian at Shaunghe and Tianba. In addition, all other recorded high Hg/TOC ratios are associated with TOC > 2.0% 22 .
A diagenetic effect is excluded because of the well-preserved conditions of primary laminated shale 4,14 . In addition, organic-carbon isotope data record the global positive excursion of the glacial interval in the Hirnantian stage, also suggesting a primary chemostratigraphic signal preserved in the sample containing matured organic matter 52 . These analyses point to no or weak diagenetic effect on our geochemical data across the O-S boundary. www.nature.com/scientificreports/ Hg enrichment pattern across the Ordovician-Silurian transition. We correlate the Hg/TOC and Hg/TS curves across the Ordovician-Silurian boundary in the three study sections, with the published Hg curves elsewhere (Fig. 4). These Hg anomalies all correspond to Hg concentration peak and peaks of Hg/TOC and/or Hg/TS ratios, indicating increase of Hg input. Two Hg positive anomalies occur in the middle and late Katian, three anomalies occur at LOMEI-1, LOMEI-2 and Late Rhuddanian, respectively (Fig. 4). Elsewhere, one Hg positive anomaly had also been found in late Katian from a drill hole XY5 in South China 23,52 and Monitor Range in North America 22 . Two Hg positive anomalies at LOMEI-1 and LOMEI-2 had also been found in many locations such as Wangjiawan, Dingjiapo 21 , XY5 drill hole 52 [21][22][23] , and large mass-independent sulfur isotope anomalies 52 . In other words, the Hg positive anomalies in the middle and late Katian suggest a volcanic increasing Hg loading during this time. High Hg/TOC or Hg/TS ratios at the LOMEI-1 at the end-Katian in the three study sections are associated with relatively high TOC or TS contents, and high Hg concentrations, also suggesting higher Hg loading into the basins. The Hg spike at the LOMEI-2 at Shuanghe was associated with high TOC contents, invariable Hg/TOC ratios & TS contents, and high Hg/TS ratios, indicating that this Hg enrichment at Shuanghe was linked to higher TOC fluxes. Meanwhile, the Hg spike at the LOMEI-2 at Qiliao was associated with high TS contents, invariable Hg/TS ratios, relatively high TOC contents and Hg/TOC ratios (Fig. 2), suggesting that Hg enrichment at Qiliao might be related to local sulfide deposition. Sulfide-carrier Hg anomaly was also reported by previous study with coarse resolution across the LOME interval 48 . Hg profile at Tianba does not show any positive anomaly at the LOMEI-2, but the good covariation of Hg-TOC (Fig. 3e) suggests organic matter carrier of Hg during this time.
Overall, Hg positive anomaly at LOMEI-1 record higher loading of Hg into the basin, while an increase of Hg drawdown at LOMEI-2 due to more reducing conditions 4 or increase of organic matter deposition in the late Hirnantian (Fig. 2). Higher Hg fluxes in the basins at LOMEI-1 could be related to different factors, as an increase of volcanic activity or enhanced continental weathering 56,57 . Considering the relatively low continental weathering indicated by chemical index alteration (CIA) values 4 and the sporadical occurrence of ash beds in South China 42,46 (Fig. 2), the abrupt Hg (and Hg/TOC) anomalies at LOMEI-1 would be of volcanic origin as suggested by previous published works in South China and U.S. [21][22][23][24] . However, intermittent or weak euxinia also developed during the LOMEI-1 4 with high Hg/TOC or Hg/TS ratios, relatively high TOC or TS contents in the three study sections, suggesting Hg enrichment during this time would be partially related to euxinic condition in water column.
The relatively high Hg concentration in the upper Rhuddanian is associated with non-euxinic conditions, relatively low TOC or TS contents, but relatively high Hg/TOC and Hg/TS ratios in this study. The abrupt increasing of Hg/TOC, or Hg/TS ratios coincides with invariable or small decreasing TOC or TS, excluding an inflation of too low TS and TOC contents. These probably suggest a genuine Hg positive anomaly and extra environmental loading related to volcanism or weathering 56,57 . This anomaly is associated with abrupt occurrence of frequent ash beds 42 in Fig. 2 and relatively low weathering of CIA evidence 10 , pointing to a volcanic origin of increasing Hg loading. Previous study 53 has also suggested that this anomaly in the Scotland derived from increased Hg flux rather than sequestration by anoxia/euxinia. These may indicate global Hg loading by volcanism during the late Rhuddanian.
Implications for the mass extinction. The interpretation of two different controls on the recorded Hg anomalies, i.e., a mixed origin of volcanism and euxinia for the Hg anomaly at the LOMEI-1 and a redox control on the Hg anomaly at the LOMEI-2, shed new lights on the Late Ordovician extinction mechanism. The middle-Katian Hg positive anomaly was temporally coincided with the middle-Katian genus richness drop 58 . The inferred volcanic-origin (although lack of solid volcanic lithology evidences) of Hg positive anomaly in the middle Katian in this study may suggest significant climatic effect triggered by volcanism on the initial of longterm mass extinction from middle Katian to late Hirnantian 58,59 .
The most distinct Hg anomaly and volcanism reported by previous studies are in the Late Katian and at LOMEI-1 (at end-Katian) (Fig. 4). As shown in Fig. 2, intensity of volcanic activity estimated by distribution and thickness of volcanic ash layers gradually decreased from the middle Katian to end-Katian. However, long-term www.nature.com/scientificreports/ weathering of volcanic deposits would enhance the nutrient input to ocean and thus result in large amount of organic matter burial and the consumption of CO 2 in the atmosphere via biological pump [59][60][61] . Increasing burial rates of organic matter would gradually contribute to expansion of euxinia in bottom water 4 , finally driving the LOMEI-1. Additionally, Hg toxic effect could also have contributed to this extinction process 57 . As shown by our data, the development of euxinic conditions at the LOMEI-2 was not related to volcanism (Fig. 2), but to the large amount of organic matter burial resulted from increased availability of nutrients either input from exposed continental shelves or recycled from organic matter degradation 4 . However, at the LOMEI-2, high organic carbon burial mentioned above created euxinic conditions in bottom water, accumulating Hg and killing the survivors such as conodonts, Hirnantia fauna (cool water brachiopod fauna) 5 after LOMEI-1.

Conclusions
We present herein five Hg anomaly enrichments across the Ordovician-Silurian boundary, i.e., two anomalies in the middle and late Katian, three anomalies at LOMEI-1 (end-Katian), LOMEI-2 (late Hirnantian), and one spike in the late Rhuddanian of South China, respectively. All these Hg anomalies in the Late Ordovician and early Silurian were global or at least regional based on the global Hg chemostratigraphy correlation. The Hg positive anomalies in the middle-late Katian and in the late Rhuddanian were probably caused by primary volcanic loading. Our data suggest that during the mass extinction interval, the Hg positive anomalies at LOMEI-1 and LOMEI-2 have been controlled by different factors: i.e., volcanism probably caused the Hg anomaly at the LOMEI-1, and the development of strong euxinic conditions increased Hg drawdown at the LOMEI-2. Volcanism during the Middle and late Katian would probably enhance the expansion of euxinia at the end of Katian by long-term weathering of volcanic deposits, and was finally responsible for the LOMEI-1. Furthermore, there was no or weak volcanic loading of Hg during the LOMEI-2. Hg enrichment during this time was related to euxinic condition in water column, suggesting that the LOMEI-2 was linked to euxinia.